Polyethyleneimine Mediated DNA Transfection in Schistosome Parasites and Regulation of the WNT Signaling Pathway by a Dominant-Negative SmMef2

PLoS Neglected Tropical Diseases

Volumn 7, Issue 7, 2013, Pages

  Liang, Shuang ^a   Knight, Matty ^b   Jolly, Emmitt R ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOCYTE ENHANCER FACTOR 2; POLYETHYLENEIMINE; PRIMER DNA;

ARTICLE; AUTOREGULATION; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; DISEASE CARRIER; DNA EXTRACTION; DNA TRANSFECTION; GENE; GENE CONSTRUCT; GENE EXPRESSION; GENETIC REGULATION; GENETIC TRANSCRIPTION; MCHERRY GENE; MOLECULAR GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SCHISTOSOMA; WESTERN BLOTTING; WNT SIGNALING PATHWAY;

EID: 84880851695     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002332     Document Type: Article

References (77)

1. Ding S, Wu X, Li G, Han M, Zhuang Y, et al. (2005) Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122: 473-483.
2. Langridge GC, Phan MD, Turner DJ, Perkins TT, Parts L, et al. (2009) Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Res 19: 2308-2316.
3. Brindley PJ, Pearce EJ, (2007) Genetic manipulation of schistosomes. Int J Parasitol 37: 465-473.
4. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J, (2006) Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6: 411-425.
5. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, et al. (2008) Helminth infections: the great neglected tropical diseases. J Clin Invest 118: 1311-1321.
6. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, et al. (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460: 352-358.
7. Protasio AV, Tsai IJ, Babbage A, Nichol S, Hunt M, et al. (2012) A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni. PLoS Negl Trop Dis 6: e1455.
8. Cheng G, Davis RE, (2007) An improved and secreted luciferase reporter for schistosomes. Mol Biochem Parasitol 155: 167-171.
9. Davis RE, Parra A, LoVerde PT, Ribeiro E, Glorioso G, et al. (1999) Transient expression of DNA and RNA in parasitic helminths by using particle bombardment. Proc Natl Acad Sci U S A 96: 8687-8692.
10. Heyers O, Walduck AK, Brindley PJ, Bleiss W, Lucius R, et al. (2003) Schistosoma mansoni miracidia transformed by particle bombardment infect Biomphalaria glabrata snails and develop into transgenic sporocysts. Exp Parasitol 105: 174-178.
11. Delcroix M, Sajid M, Caffrey CR, Lim KC, Dvorak J, et al. (2006) A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. J Biol Chem 281: 39316-39329.
12. Stefanic S, Dvorak J, Horn M, Braschi S, Sojka D, et al. (2010) RNA interference in Schistosoma mansoni schistosomula: selectivity, sensitivity and operation for larger-scale screening. PLoS Negl Trop Dis 4: e850.
13. Tran MH, Freitas TC, Cooper L, Gaze S, Gatton ML, et al. (2010) Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover. PLoS Pathog 6: e1000840.
14. Ayuk MA, Suttiprapa S, Rinaldi G, Mann VH, Lee CM, et al. (2011) Schistosoma mansoni U6 gene promoter-driven short hairpin RNA induces RNA interference in human fibrosarcoma cells and schistosomules. Int J Parasitol 41: 783-789.
15. Correnti JM, Jung E, Freitas TC, Pearce EJ, (2007) Transfection of Schistosoma mansoni by electroporation and the description of a new promoter sequence for transgene expression. Int J Parasitol 37: 1107-1115.
16. Krautz-Peterson G, Radwanska M, Ndegwa D, Shoemaker CB, Skelly PJ, (2007) Optimizing gene suppression in schistosomes using RNA interference. Mol Biochem Parasitol 153: 194-202.
17. Yuan XS, Shen JL, Wang XL, Wu XS, Liu DP, et al. (2005) Schistosoma japonicum: a method for transformation by electroporation. Exp Parasitol 111: 244-249.
18. Beckmann S, Buro C, Dissous C, Hirzmann J, Grevelding CG, (2010) The Syk kinase SmTK4 of Schistosoma mansoni is involved in the regulation of spermatogenesis and oogenesis. PLoS Pathog 6: e1000769.
19. Nabhan JF, El-Shehabi F, Patocka N, Ribeiro P, (2007) The 26S proteasome in Schistosoma mansoni: bioinformatics analysis, developmental expression, and RNA interference (RNAi) studies. Exp Parasitol 117: 337-347.
20. Duvoisin R, Ayuk MA, Rinaldi G, Suttiprapa S, Mann VH, et al. (2012) Human U6 promoter drives stronger shRNA activity than its schistosome orthologue in Schistosoma mansoni and human fibrosarcoma cells. Transgenic Res 21: 511-521.
21. Kines KJ, Morales ME, Mann VH, Gobert GN, Brindley PJ, (2008) Integration of reporter transgenes into Schistosoma mansoni chromosomes mediated by pseudotyped murine leukemia virus. FASEB J 22: 2936-2948.
22. Kalinna BH, Brindley PJ, (2007) Manipulating the manipulators: advances in parasitic helminth transgenesis and RNAi. Trends Parasitol 23: 197-204.
23. Correnti JM, Brindley PJ, Pearce EJ, (2005) Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Mol Biochem Parasitol 143: 209-215.
24. Rossi A, Wippersteg V, Klinkert MQ, Grevelding CG, (2003) Cloning of 5′ and 3′ flanking regions of the Schistosoma mansoni calcineurin A gene and their characterization in transiently transformed parasites. Mol Biochem Parasitol 130: 133-138.
25. Wippersteg V, Kapp K, Kunz W, Grevelding CG, (2002) Characterisation of the cysteine protease ER60 in transgenic Schistosoma mansoni larvae. Int J Parasitol 32: 1219-1224.
26. Wippersteg V, Kapp K, Kunz W, Jackstadt WP, Zahner H, et al. (2002) HSP70-controlled GFP expression in transiently transformed schistosomes. Mol Biochem Parasitol 120: 141-150.
27. Correnti JM, Pearce EJ, (2004) Transgene expression in Schistosoma mansoni: introduction of RNA into schistosomula by electroporation. Mol Biochem Parasitol 137: 75-79.
28. Tchoubrieva EB, Ong PC, Pike RN, Brindley PJ, Kalinna BH, (2010) Vector-based RNA interference of cathepsin B1 in Schistosoma mansoni. Cell Mol Life Sci 67: 3739-3748.
29. Zhao ZR, Lei L, Liu M, Zhu SC, Ren CP, et al. (2008) Schistosoma japonicum: inhibition of Mago nashi gene expression by shRNA-mediated RNA interference. Exp Parasitol 119: 379-384.
30. Yuan XS, Shen JL, Wang XL, Hu YS, Luo QL, (2005) [Transformation of schistosomulae by electroporation and transient expression of the enhanced green fluorescent protein (EGFP) gene]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 23: 202-205.
31. Weaver JC, (1995) Electroporation theory. Concepts and mechanisms. Methods Mol Biol 48: 3-28.
32. Maule AG, Marks NJ (2006) Parasitic flatworms: molecular biology, biochemistry, immunology and physiology. Wallingford, UK; Cambridge, MA: CABI. xx, 448 p. p.
33. Boussif O, Lezoualc'h F, Zanta MA, Mergny MD, Scherman D, et al. (1995) A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci U S A 92: 7297-7301.
34. Dunlap DD, Maggi A, Soria MR, Monaco L, (1997) Nanoscopic structure of DNA condensed for gene delivery. Nucleic Acids Res 25: 3095-3101.
35. Godbey WT, Barry MA, Saggau P, Wu KK, Mikos AG, (2000) Poly(ethylenimine)-mediated transfection: a new paradigm for gene delivery. J Biomed Mater Res 51: 321-328.
36. Godbey WT, Wu KK, Hirasaki GJ, Mikos AG, (1999) Improved packing of poly(ethylenimine)/DNA complexes increases transfection efficiency. Gene Ther 6: 1380-1388.
37. Godbey WT, Wu KK, Mikos AG, (1999) Tracking the intracellular path of poly(ethylenimine)/DNA complexes for gene delivery. Proc Natl Acad Sci U S A 96: 5177-5181.
38. Knight M, Miller A, Liu Y, Scaria P, Woodle M, et al. (2011) Polyethyleneimine (PEI) mediated siRNA gene silencing in the Schistosoma mansoni snail host, Biomphalaria glabrata. PLoS Negl Trop Dis 5: e1212.
39. Wiseman JW, Goddard CA, McLelland D, Colledge WH, (2003) A comparison of linear and branched polyethylenimine (PEI) with DCChol/DOPE liposomes for gene delivery to epithelial cells in vitro and in vivo. Gene Ther 10: 1654-1662.
40. Milligan JN, Jolly ER, (2012) Identification and characterization of a Mef2 transcriptional activator in schistosome parasites. PLoS Negl Trop Dis 6: e1443.
41. Potthoff MJ, Olson EN, (2007) MEF2: a central regulator of diverse developmental programs. Development 134: 4131-4140.
42. Clevers H, Nusse R, (2012) Wnt/beta-catenin signaling and disease. Cell 149: 1192-1205.
43. Lim X, Nusse R, (2012) Wnt Signaling in Skin Development, Homeostasis, and Disease. Cold Spring Harb Perspect Biol.
44. van Amerongen R, Nusse R, (2009) Towards an integrated view of Wnt signaling in development. Development 136: 3205-3214.
45. Li HF, Wang XB, Jin YP, Xia YX, Feng XG, et al. (2010) Wnt4, the first member of the Wnt family identified in Schistosoma japonicum, regulates worm development by the canonical pathway. Parasitol Res 107: 795-805.
46. Parker-Manuel SJ, Ivens AC, Dillon GP, Wilson RA, (2011) Gene expression patterns in larval Schistosoma mansoni associated with infection of the mammalian host. PLoS Negl Trop Dis 5: e1274.
47. Wang X, Li H, Qi X, Shi Y, Xia Y, et al. (2011) Characterization and expression of a novel Frizzled 9 gene in Schistosoma japonicum. Gene Expr Patterns 11: 263-270.
48. Basch PF, (1981) Cultivation of Schistosoma mansoni in vitro. I. Establishment of cultures from cercariae and development until pairing. J Parasitol 67: 179-185.
49. Milligan JN, Jolly ER, (2011) Cercarial transformation and in vitro cultivation of Schistosoma mansoni schistosomules. J Vis Exp (54) pp. 3191 doi: 10.3791/3191.
50. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402-408.
51. Goula D, Benoist C, Mantero S, Merlo G, Levi G, et al. (1998) Polyethylenimine-based intravenous delivery of transgenes to mouse lung. Gene Ther 5: 1291-1295.
52. Goula D, Remy JS, Erbacher P, Wasowicz M, Levi G, et al. (1998) Size, diffusibility and transfection performance of linear PEI/DNA complexes in the mouse central nervous system. Gene Ther 5: 712-717.
53. Reed SE, Staley EM, Mayginnes JP, Pintel DJ, Tullis GE, (2006) Transfection of mammalian cells using linear polyethylenimine is a simple and effective means of producing recombinant adeno-associated virus vectors. J Virol Methods 138: 85-98.
54. Moghimi SM, Symonds P, Murray JC, Hunter AC, Debska G, et al. (2005) A two-stage poly(ethylenimine)-mediated cytotoxicity: implications for gene transfer/therapy. Mol Ther 11: 990-995.
55. Zhao QQ, Chen JL, Lv TF, He CX, Tang GP, et al. (2009) N/P ratio significantly influences the transfection efficiency and cytotoxicity of a polyethylenimine/chitosan/DNA complex. Biol Pharm Bull 32: 706-710.
56. Choosakoonkriang S, Lobo BA, Koe GS, Koe JG, Middaugh CR, (2003) Biophysical characterization of PEI/DNA complexes. J Pharm Sci 92: 1710-1722.
57. Schiffelers RM, Ansari A, Xu J, Zhou Q, Tang Q, et al. (2004) Cancer siRNA therapy by tumor selective delivery with ligand-targeted sterically stabilized nanoparticle. Nucleic Acids Res 32: e149.
58. Osman A, Niles EG, Verjovski-Almeida S, LoVerde PT, (2006) Schistosoma mansoni TGF-beta receptor II: role in host ligand-induced regulation of a schistosome target gene. PLoS Pathog 2: e54.
59. Koster B, Strand M, (1994) Schistosoma mansoni: Sm23 is a transmembrane protein that also contains a glycosylphosphatidylinositol anchor. Arch Biochem Biophys 310: 108-117.
60. Reynolds SR, Shoemaker CB, Harn DA, (1992) T and B cell epitope mapping of SM23, an integral membrane protein of Schistosoma mansoni. J Immunol 149: 3995-4001.
61. Black BL, Olson EN, (1998) Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu Rev Cell Dev Biol 14: 167-196.
62. Naya FJ, Olson E, (1999) MEF2: a transcriptional target for signaling pathways controlling skeletal muscle growth and differentiation. Curr Opin Cell Biol 11: 683-688.
63. Snyder CM, Rice AL, Estrella NL, Held A, Kandarian SC, et al. (2013) MEF2A regulates the Gtl2-Dio3 microRNA mega-cluster to modulate WNT signaling in skeletal muscle regeneration. Development 140: 31-42.
64. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
65. Ramachandran B, Yu G, Li S, Zhu B, Gulick T, (2008) Myocyte enhancer factor 2A is transcriptionally autoregulated. J Biol Chem 283: 10318-10329.
66. Lutz GJ, Sirsi SR, Williams JH, (2008) PEG-PEI copolymers for oligonucleotide delivery to cells and tissues. Methods Mol Biol 433: 141-158.
67. Ogris M, Walker G, Blessing T, Kircheis R, Wolschek M, et al. (2003) Tumor-targeted gene therapy: strategies for the preparation of ligand-polyethylene glycol-polyethylenimine/DNA complexes. J Control Release 91: 173-181.
68. Ornatsky OI, Andreucci JJ, McDermott JC, (1997) A dominant-negative form of transcription factor MEF2 inhibits myogenesis. J Biol Chem 272: 33271-33278.
69. Gregoire S, Tremblay AM, Xiao L, Yang Q, Ma K, et al. (2006) Control of MEF2 transcriptional activity by coordinated phosphorylation and sumoylation. J Biol Chem 281: 4423-4433.
70. Lu J, McKinsey TA, Nicol RL, Olson EN, (2000) Signal-dependent activation of the MEF2 transcription factor by dissociation from histone deacetylases. Proc Natl Acad Sci U S A 97: 4070-4075.
71. Molkentin JD, Li L, Olson EN, (1996) Phosphorylation of the MADS-Box transcription factor MEF2C enhances its DNA binding activity. J Biol Chem 271: 17199-17204.
72. Zhao M, New L, Kravchenko VV, Kato Y, Gram H, et al. (1999) Regulation of the MEF2 family of transcription factors by p38. Mol Cell Biol 19: 21-30.
73. Zhao P, Hoffman EP, (2004) Embryonic myogenesis pathways in muscle regeneration. Dev Dyn 229: 380-392.
74. Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, et al. (2006) The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38: 228-233.
75. Chen Z, Liang S, Zhao Y, Han Z, (2012) miR-92b regulates Mef2 levels through a negative-feedback circuit during Drosophila muscle development. Development 139: 3543-3552.
76. Haberland M, Arnold MA, McAnally J, Phan D, Kim Y, et al. (2007) Regulation of HDAC9 gene expression by MEF2 establishes a negative-feedback loop in the transcriptional circuitry of muscle differentiation. Mol Cell Biol 27: 518-525.
77. Sandmann T, Jensen LJ, Jakobsen JS, Karzynski MM, Eichenlaub MP, et al. (2006) A temporal map of transcription factor activity: mef2 directly regulates target genes at all stages of muscle development. Dev Cell 10: 797-807.